Foreign exploration for Asian natural enemies of BMSB (2007-2015)
30+ parasitoid populations in
culture at ARS BIIR for host range
and efficacy testing
tsp180
tsp181
tsp179
tsp175
tsp174
tsp173
tsp172
tsp171
tsp169
tsp168
tsp166
tsp165
tsp164
tsp163
tsp157
TSP130
TSp125
TSp118
TSP115
TSp110
Tsp53
TSP98
TSp102
TSp106
Tsp50
Tsp49
Tsp48
Tsp45
Tsp44
tsp185
TSP77
TSP78
TSP79
TSP88
TSP90
TSP91
TSP93
Tsp52
Tsp41
tsp154
tsp155
tsp167
tsp170
tsp182
TSP144
TSP141
TSP142
TSP143
TSP145
TSP146
TSP147
TSP148
Tsp51
tsp186
Tsp43
tsp161
tsp176
Tsp42
Tsp46
tsp162
Tsp54
TSP127
TSP128
TSp126
TSP96
TSP92
TSP87
TSP86
TSP84
TSP83
TSP82
TSP80
TSP81
TSP85
TSP89
TSP129
TSP131
TSP132
TSP133
TSP134
TSP135
TSP136
TSP137
TSP138
TSP139
TSP140
Tsp40
Tsp58
Tsp59
TSP94
TSP95
TSP152
TSP153
TSP151
TSP150
TSP149
Tsp39
tsp189
tsp184
tsp188
tsp156
tsp177
tsp178
tsp187
tsp190
tsp191
tsp183
Tsp55
Tsp57
tsp192
tsp193
tsp194
tsp159
tsp158
tsp160100
73
99
100
100
100
100
100
100
100
100
100
100
100
61
61
100
83
62
99
77
100
76
26
41
5
1
22
58
85
100
100
100
99
100
59
69
0.1
Phylogenetic treebased on
Maximum Likelihood, GTR+G+I model
(CO1)T. japonicus
T. spp.
Gryon sp.
T. mitsukurii
T. cultratus
T. plautiae
T. edessae
T. spp.
T. spp.
Telenomus spp.
Contributors:M.-C. Bon – ARS/EBCLE. Talamas – ARS/SELM. Buffington – ARS/SELC. Dieckhoff – ARS/BIIRK. Hoelmer – ARS/BIIR
Scelionidae recovered from Asian Pentatomid eggs
&
Scelionidae recovered from NorthAmerican Pentatomid eggs
Trissolcus japonicus (Hymenoptera: Scelionidae)
(first described as T. halyomorphae)
solitary egg parasitoid
2 - 3 weeks/generation
multiple generations/season
female-biased sex ratio
65 to 90% parasitism on BMSB
reported in Asia
Yang et al. (2009) Annals of the Entomological Society of America . 102: 39-47
Brian T. Cutting
Trissolcus japonicus is oligophagous - it attacks several Asian pentatomid species
Dolycoris baccarumPlautia crossota
Glaucias subpunctatus
Erthesina fullo
Halyomorpha halys
Funding for Host Range Evaluations:
Farm Bill funding (APHIS PPQ)
NIFA SCRI multi-institution BMSB grant
Collaborators:USDA-ARS (Newark, DE & EBCL, France)
University of Delaware (D. Tallamy)
Florida Dept. Agriculture & Consumer Services, Division of Plant Industry
MSU – Michigan State University – Department of Entomology (E. Delfosse)
Oregon Department of Agriculture
Oregon State University – Department of Horticulture (V. Walton, P. Shearer)
University of California, Riverside & CDFA (M. Hoddle, C. Pickett)
Host Range Evaluations– A team effort to fast-track the evaluation process
FL
MI
OR
DECA
= active screening for 2+ yrs
= started 2013
= started 2014
Host Range Evaluations: Progress
0 17.5 35 52.5 70
40 species in progress
62 species total tested nationwide
22 species completed
No Choice Test
Followed by a BMSB target egg mass as control for another 24h:
Exposure to non-target species egg mass only – for 24h:
Choice Test
Egg masses of non-target species and BMSB presented together for 24h: If parasitism
on non-target is recorded
Host range testing procedures
No-Choice Test Outcome - Part 1 (as of 2015)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Trichopepla semivittata (N=)
Thyanta pallidovirens (N=16)
Stiretrus anchorago (N=6)
Podisus brevispinus (N=9)
Perillus bioculatus (N=7)
Oebalus pugnax (N=12)
Murgantia histrionica (N=23)
Holcostethus abbreviatus (N=20)
Edessa florida (N=28)
Cosmopepla intergressa (N=5)
Coleotichus blackburniae KOA (N=12)
Coenus delius (N=12)
Chlorochroa ligata (N=25)
Brochymena quadripustulata (N=17)
Bagrada hilaris (N=7)
Antheminia remota (N=6)
Amaurochrous sp. (N=8)
Agonoscelis puberula (N=12)
live males live females unemerged parasitoids hatched nymphs unhatched nymphs
No-Choice Test Outcome - Part 2 (as of 2015)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Thyanta custator accerra (MI, N=22)
Thyanta custator accerra (DE, N=13)
Thyanta custator (OR, N=23)
Thyanta custator (DE, N=23)
Podisus maculiventris (MI, N=19)
Podisus maculiventris (DE, N=34)
Holcostethus limbolarius (MI, N=20)
Holcostethus limbolarius (DE, N=20)
Euschistus variolarius (DE, N=21)
Euschistus variolarius (MI, N=17)
Euschistus tristigmus luridus (MI, N=20)
Euschistus tristigmus (DE, N=26)
Euschistus servus euschistoides (MI, N=13)
Euschistus servus (DE, N=20)
Cosmopepla lintneriana (OR, N=16)
Cosmopepla lintneriana (DE, N=26)
Chlorochroa uhleri (OR, N=8)
Chlorochroa uhleri (CA, N=8)
Chinavia hilaris (OR, N=19)
Chinavia hilaris (MI, N=17)
Banasa dimiata (OR, N=22)
Banasa dimiata (MI, N=13)
live males live females unemerged parasitoids hatched nymphs unhatched nymphs
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Stiretrus anchorago (N=6)
BMSB
Podisus maculiventris (N=31)
BMSB
Murgantia histrionica (N=27)
BMSB
Euschistus servus (N=25)
BMSB
Edessa florida (N=21)
BMSB
Chlorochroa ligata (N=18)
BMSB
Chinavia hilaris (N=23)
BMSB
Banasa dimiata (N=33)
BMSB
live males live females unemerged parasitoids hatched nymphs unhatched nymphs
Choice Test Outcome - Part 1 (as of 2015)
Choice Test Outcome - Part 2 (as of 2015)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Thyanta custator accerra (MI, N=28)
BMSB
Thyanta custator (DE, N=35)
BMSB
Thyanta custator (OR, N=26)
BMSB
Holcostethus limbolaris (DE, N=10)
BMSB
Holcostethus limbolaris (MI, N=21)
BMSB
Euschistus variolarius (DE, N=17)
BMSB
Euschistus variolarius (MI, N=9)
BMSB
Euschistus tristigmus (DE, N=25)
BMSB
Euschistus tristigmus luridus (MI, N=8)
BMSB
Cosmopepla lintneriana (DE, N=12)
BMSB
Cosmopepla lintneriana (MI, N=22)
BMSB
live males live females unemerged parasitoids hatched nymphs unhatched nymphs
Influence of time of exposure
Finishedo 1 ho 4 ho 6 ho 24 h
Behavioral observations
Arena
Egg mass Ongoingo Searching behavioro Oviposition behavioro Host choiceo …
Influence of arena size and complexity
Size (Finished)o 10 dramo 100 dramo 500 dramo 1000 dramo 2000 dram
Complexity (Started)o Choice tests on plants
Role of parasitoid physiology & experience
o Parental experienceo Parental physiologyo Effect of host choice on
offspring physiology & behavior
A Closer Look at Host Choice Behavior in T. japonicus
www.ars-fla.com
Olfactometer Studies(FL, MI) - ongoing
Recovery of Trissolcus japonicus in Maryland in 2014
a potential game changer?
Photo: E. Talamas ARS/SEL
Genetic distance between populations
Co
ord
. 2
Coord. 1
DC area recoveries
Vancouver WA recovery
Japan
ChinaSouth Korea
Axis 1 & axis 2 explain, 22% and 20% respectively, of the distribution
Beijing
Origin of the adventive T. japonicus populations
Principal coordinates analysis of genetic diversity among 23 microsatellite markers in T. japonicus
Take home message:
1) These populations are adventive – they were not released nor did they escape quarantine!
2) DC area populations genetically similar to populations sampled in Japan and S. Korea
3) WA population genetically similar to populations sampled in S. Korea
Quarantine Host Range Evaluations:• Continue laboratory host range research (pending evidence of establishment and dispersal of
adventive populations) towards a Petition to Release (APHIS requires a Petition to Release for each state)
Adventive Trissolcus japonicus: • Expand surveys initiated in 2015 to determine the extent of establishment, incl. an increased
focus on wooded habitats and a widened survey area to see how quickly populations spread
• Analyze recovered parasitoid microsatellite DNA to determine heterogeneity of the adventive populations
• Increase monitoring of parasitism of BMSB & non-target pentatomid egg masses in the field
Logical next steps – Asian Natural Enemies